Meiotic maturation of incompetent prepubertal sheep oocytes is induced by paracrine factor(s) released by gonadotropin-stimulated oocyte-cumulus cell complexes and involves mitogen-activated protein kinase activation

Endocrinology

Volumn 149, Issue 1, 2008, Pages 100-107

  Cecconi, Sandra ^a   Mauro, Annunziata ^b   Capacchietti, Giulia ^b   Berardinelli, Paolo ^b   Bernabò, Nicola ^b   Di Vincenzo, Anna Rita ^b   Mattioli, Mauro ^b   Barboni, Barbara ^b  

^a UNIVERSITY OF L'AQUILA   (Italy)

^b UNIVERSITY OF TERAMO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLITROPIN; GONADOTROPIN; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL CYCLE ARREST; CELL STIMULATION; COCULTURE; CONTROLLED STUDY; CUMULUS OOPHORUS; DEVELOPMENTAL STAGE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMALE; GERM CELL; GRANULOSA CELL; HORMONE ACTION; IN VITRO STUDY; MEIOSIS; METAPHASE; NONHUMAN; OOCYTE MATURATION; PARACRINE SIGNALING; PREPUBERTY; PRIORITY JOURNAL; SHEEP; SOMATIC CELL;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CUMULUS CELLS; ENZYME ACTIVATION; FEMALE; GONADOTROPINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MAP KINASE KINASE KINASES; MEIOSIS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; OOCYTES; OOGENESIS; SHEEP;

EID: 37549030567     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2007-0874     Document Type: Article

References (57)

1. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A 2002 Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61:414-424
2. Buccione R, Schroeder AC, Eppig JJ 1990 Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 43:543-547
3. Cecconi S, Ciccarelli C, Barberi M, Macchiarelli G, Canipari R 2004 Granulosa cell-oocyte interactions. Eur J Obstet Gynecol Reprod Biol 115(Suppl 1):S19-S22
4. Eppig JJ 2001 Oocyte control of ovarian follicular development and function in mammals. Reproduction 122:829-838
5. Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ 2001 Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 121:647-653
6. Gilchrist RB, Ritter LJ, Armstrong DT 2004 Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 82-83:431-446
7. Matzuk MM, Burns KH, Viveiros MM, Eppig JJ 2002 Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 296:2178-2180
8. Bao S, Ushijima H, Hirose A, Aono F, Ono Y, Kono T 2003 Development of bovine oocytes reconstructed with a nucleus from growing stage oocytes after fertilization in vitro. Theriogenology 59:1231-1239
9. Eppig JJ 1996 Coordination of nuclear and cytoplasmic oocyte maturation in eutherian mammals. Reprod Fertil Dev 8:485-489
10. Mattson BA, Albertini DF 1990 Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol Reprod Dev 25:374-383
11. Connors SA, Kanatsu-Shinohara M, Schultz RM, Kopf GS 1998 Involvement of the cytoskeleton in the movement of cortical granules during oocyte maturation, and cortical granule anchoring in mouse eggs. Dev Biol 200:103-115
12. Eppig JJ, Viveiros MM, Bivens CM, De La Fuente R 2004 Regulation of mammalian oocyte maturation. Ovary 71:113-11129
13. Pincus G, Enzmann EV 1935 The comparative behaviour of mammalian eggs in vivo and in vitro. I. The activation of ovarian eggs. J Exp Med 84:655-1054
14. Mehlmann LM, Jones TL, Jaffe LA 2002 Meiotic arrest in the mouse follicle maintained by a Gs protein in the oocyte. Science 297:1343-1345
15. Moor RM, Trounson AO 1977 Hormonal and follicular factors affecting maturation of sheep oocytes in vitro and their subsequent developmental capacity. J Reprod Fertil 49:101-109
16. 2+ during oocyte maturation. J Reprod Fertil 118:337-342
17. Downs SM, Daniel SA, Eppig JJ 1988 Induction of maturation in cumulus cell-enclosed mouse oocytes by follicle-stimulating hormone and epidermal growth factor: evidence for a positive stimulus of somatic cell origin. J Exp Zool 245:86-96
18. Fan HY, Huo LJ, Chen DY, Schatten H, Sun QY 2004 Protein kinase C and mitogen-activated protein kinase cascade in mouse cumulus cells: cross talk and effect on meiotic resumption of oocyte. Biol Reprod 70:1178-1187
19. Mattioli M 1994 Transduction mechanisms for gonadotrophin-induced oocyte maturation in mammals. Zygote 2:347-349
20. Fan HY, Tong C, Lian L, Li SW, Gao WX, Cheng Y, Chen DY, Schatten H, Sun QY 2003 Characterization of ribosomal S6 protein kinase p90rsk during meiotic maturation and fertilization in pig oocytes: mitogen-activated protein kinase-associated activation and localization. Biol Reprod 68:968-977
21. Ohashi S, Naito K, Sugiura K, Iwamori N, Goto S, Naruoka H, Tojo H 2003 Analyses of mitogen-activated protein kinase function in the maturation of porcine oocytes. Biol Reprod 68:604-609
22. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2002 Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143:2221-2232
23. Su YQ, Denegre JM, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2003 Oocyte-dependent activation of mitogen-activated protein kinase (ERK1/2) in cumulus cells is required for the maturation of the mouse oocyte-cumulus cell complex. Dev Biol 263:126-138
24. Tsafriri A, Cao X, Ashkenazi H, Motola S, Popliker M, Pomerantz SH 2005 Resumption of oocyte meiosis in mammals: on models, meiosis activating sterols, steroids and EGF-like factors. Mol Cell Endocrinol 234:37-45
25. Fan HY, Sun QY 2004 Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol Reprod 70:535-547
26. Su YQ, Rubinstein S, Luria A, Lax Y, Breitbart H 2001 Involvement of MEK-mitogen-activated protein kinase pathway in follicle-stimulating hormone-induced but not spontaneous meiotic resumption of mouse oocytes. Biol Reprod 65:358-365
27. Liang CG, Huo LJ, Zhong ZS, Chen DY, Schatten H, Sun QY 2005 Cyclic adenosine 3′,5′-monophosphate-dependent activation of mitogen-activated protein kinase in cumulus cells is essential for germinal vesicle breakdown of porcine cumulus-enclosed oocytes. Endocrinology 146:4437-4444
28. Conti M, Hsieh M, Park JY, Su YQ 2006 Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol 20:715-723
29. Diaz FJ, O'Brien MJ, Wigglesworth K, Eppig JJ 2006 The preantral granulosa cell to cumulus cell transition in the mouse ovary: development of competence to undergo expansion. Dev Biol 299:91-104
30. Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ 1990 Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 140:307-317
31. Ochsner SA, Day AJ, Rugg MS, Breyer RM, Gomer RH, Richards JS 2003 Disrupted function of tumor necrosis factor-α-stimulated gene 6 blocks cumulus cell-oocyte complex expansion. Endocrinology 144:4376-4384
32. Ochsner SA, Russell DL, Day AJ, Breyer RM, Richards JS 2003 Decreased expression of tumor necrosis factor-α-stimulated gene 6 in cumulus cells of the cyclooxygenase-2 and EP2 null mice. Endocrinology 144:1008-1019
33. Prochazka R, Nagyova E, Brem G, Schellander K, Motlik J 1998 Secretion of cumulus expansion-enabling factor (CEEF) in porcine follicles. Mol Reprod Dev 49:141-149
34. Ledda S, Bogliolo L, Leoni G, Naitana S 1999 Follicular size affects the meiotic competence of in vitro matured prepubertal and adult oocytes in sheep. Reprod Nutr Dev 39:503-508
35. Hunter MG, Robinson RS, Mann GE, Webb R 2004 Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim Reprod Sci 82-83:461-477
36. Buccione R, Vanderhyden BC, Caron PJ, Eppig JJ 1990 FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol 138:16-25
37. Ledda S, Bogliolo L, Leoni G, Naitana S 2001 Cell coupling and maturation-promoting factor activity in in vitro-matured prepubertal and adult sheep oocytes. Biol Reprod 65:247-252
38. Lowry Oh, Rosebrough Nj, Farr Al, Randall RJ 1951 Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
39. Denhardt DT 1996 Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiplex signalling. Biochem J 318(Pt 3):729-747
40. Hampl A, Eppig JJ 1995 Analysis of the mechanism(s) of metaphase I arrest in maturing mouse oocytes. Development 121:925-933
41. Sedmikova M, Burdova J, Petr J, Etrych M, Rozinek J, Jilek F 2003 Induction and activation of meiosis and subsequent parthenogenetic development of growing pig oocytes using calcium ionophore A23187. Theriogenology 60:1609-1620
42. Downs SM, Mastropolo AM 1994 The participation of energy substrates in the control of meiotic maturation in murine oocytes. Dev Biol 162:154-168
43. Downs SM 2001 A gap-junction-mediated signal, rather than an external paracrine factor, predominates during meiotic induction in isolated mouse oocytes. Zygote 9:71-82
44. Nagyova E, Vanderhyden BC, Prochazka R 2000 Secretion of paracrine factors enabling expansion of cumulus cells is developmentally regulated in pig oocytes. Biol Reprod 63:1149-1156
45. Prochazka R, Nagyova E, Rimkevicova Z, Nagai T, Kikuchi K, Motlik J 1991 Lack of effect of oocytectomy on expansion of the porcine cumulus. J Reprod Fertil 93:569-576
46. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB 2007 Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 76:848-857
47. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ 2004 Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte-granulosa cell regulatory loop. Dev Biol 276:64-73
48. Latham KE, Wigglesworth K, McMenamin M, Eppig JJ 2004 Stage-dependent effects of oocytes and growth differentiation factor 9 on mouse granulosa cell development: advance programming and subsequent control of the transition from preantral secondary follicles to early antral tertiary follicles. Biol Reprod 70:1253-1262
49. Abrieu A, Doree M, Fisher D 2001 The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J Cell Sci 114:257-267
50. Calder MD, Caveney AN, Smith LC, Watson AJ 2003 Responsiveness of bovine cumulus-oocyte-complexes (COC) to porcine and recombinant human FSH, and the effect of COC quality on gonadotropin receptor and Cx43 marker gene mRNAs during maturation in vitro. Reprod Biol Endocrinol 1:14
51. van Tol HT, van Eijk MJ, Mummery CL, van den HR, Bevers MM 1996 Influence of FSH and hCG on the resumption of meiosis of bovine oocytes surrounded by cumulus cells connected to membrana granulosa. Mol Reprod Dev 45:218-224
52. Hoshino Y, Yokoo M, Yoshida N, Sasada H, Matsumoto H, Sato E 2004 Phosphatidylinositol 3-kinase and Akt participate in the FSH-induced meiotic maturation of mouse oocytes. Mol Reprod Dev 69:77-86
53. Xie H, Xia G, Byskov AG, Andersen CY, Bo S, Tao Y 2004 Roles of gonadotropins and meiosis-activating sterols in meiotic resumption of cultured follicle-enclosed mouse oocytes. Mol Cell Endocrinol 218:155-163
54. Marangos P, Verschuren EW, Chen R, Jackson PK, Carroll J 2007 Prophase I arrest and progression to metaphase I in mouse oocytes are controlled by Emi1-dependent regulation of APC(Cdh1). J Cell Biol 176:65-75
55. Motlik J, Kubelka M 1990 Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol Reprod Dev 27:366-375
56. Cecconi S, Capacchietti G, Russo V, Berardinelli P, Mattioli M, Barboni B 2004 In vitro growth of preantral follicles isolated from cryopreserved ovine ovarian tissue. Biol Reprod 70:12-17
57. Thomas FH, Walters KA, Telfer EE 2003 How to make a good oocyte: an update on in-vitro models to study follicle regulation. Hum Reprod Update 9:541-555